Divergence in Male and Female Manipulative Behaviors with the Intensification of Metallurgy in...

Divergence in Male and Female Manipulative Behaviorswith the Intensification of Metallurgy in Central EuropeAlison A. Macintosh1*, Ron Pinhasi2, Jay T. Stock1

1 PAVE Research Group, Department of Archaeology and Anthropology, University of Cambridge, Cambridge, United Kingdom, 2 Earth Institute and School of

Archaeology, Newman Building, University College Dublin, Dublin, Ireland

Abstract

Humeral morphology has been shown to reflect, in part, habitual manipulative behaviors in humans. Among CentralEuropean agricultural populations, long-term social change, increasing task specialization, and technological innovation allhad the potential to impact patterns of habitual activity and upper limb asymmetry. However, systematic temporal changein the skeletal morphology of agricultural populations in this region has not been well-characterized. This study investigatesdiachronic patterns in humeral biomechanical properties and lengths among 174 adult Central European agriculturaliststhrough the first ,5400 years of farming in the region. Greater asymmetry in biomechanical properties was expected toaccompany the introduction of metallurgy, particularly in males, while upper limb loading patterns were expected to bemore similar between the Bronze and Iron Ages. Results revealed a divergence in the lateralization of upper limbbiomechanical properties by sex between the Early/Middle Neolithic and Early/Middle Bronze Age. Neolithic females hadsignificantly more variable properties than males in both humeri, while Bronze Age female properties becamehomogeneous and very symmetrical relative to the right-biased lateralization of contemporaneous males. The BronzeAge to Iron Age transition was associated with morphological change among females, with a significant increase in right-biased asymmetry and a concomitant reduction in sexual dimorphism. Relative to biomechanical properties, humeral lengthvariation and asymmetry were low though some significant sexual dimorphism and temporal change was found. It wasamong females that the lateralization of humeral biomechanical properties, and variation within them, changed mostprofoundly through time. This suggests that the introduction of the ard and plow, metallurgical innovation, taskspecialization, and socioeconomic change through ,5400 years of agriculture impacted upper limb loading in CentralEuropean women to a greater extent than men.

Citation: Macintosh AA, Pinhasi R, Stock JT (2014) Divergence in Male and Female Manipulative Behaviors with the Intensification of Metallurgy in CentralEurope. PLoS ONE 9(11): e112116. doi:10.1371/journal.pone.0112116

Editor: Clark Spencer Larsen, Ohio State University, United States of America

Received July 12, 2014; Accepted October 12, 2014; Published November 12, 2014

Copyright: � 2014 Macintosh et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permitsunrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. The data used in this study is available eitherwithin the paper or in its Supporting Information file.

Funding: The authors were funded by the following: Cambridge Commonwealth, European and International Trust (AAM) (http://www.cambridgetrust.org/);Social Sciences and Humanities Research Council of Canada (AAM) (http://www.sshrc-crsh.gc.ca/); and European Research Council Starting Grant ERC-2010-StG263,441 (RP) (http://erc.europa.eu/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of themanuscript.

Competing Interests: The authors have declared that no competing interests exist.

* Email: [email protected]

Introduction

The biomechanics of the human upper limb are complex;

largely free from weight bearing activities, the arms can be

employed both unilaterally and bilaterally in a wide variety of

ways. As the relationships between upper limb morphology,

biomechanics, and manipulative behaviors are complex, inter-

preting morphology in the context of cultural change in the past

can be challenging. A single dominant activity has the potential to

obscure the influence of multiple less-dominant behaviors [1–13].

Yet, the habitual performance of a wide variety of behaviors, with

no single dominant one, can also drive bone morphological

change [14]. The interpretation of upper limb biomechanics

following the transition to farming is particularly complex:

technological developments, increasing socioeconomic complexity,

and changing divisions of labor following the emergence of

agriculture likely drove increasing diversity of manual activity at

both the individual and population levels. In past agricultural

populations, low humeral asymmetry in some individuals has been

attributed to the bilateral loading associated with agricultural

activities such as the grinding of grain and maize and/or the use of

bimanual tools [15–19]. Yet marked lateralization has also been

documented, which may be the result of unilateral loading

associated with the manufacture and use of many stone, bone, and

metal tools and weapons [17,19–22]. Marked lateralization has

also been documented in living agropastoralists performing

physically demanding fieldwork from adolescence without mech-

anization [23].

Complexity in patterns of bone adaptation within and among

agriculturalist groups is also associated with increasing social

complexity through time. A comparison of two Italian agricultural

populations with similar subsistence activities but different socioeco-

nomic structure (Neolithic (,6000-5500 BP) versus Iron Age

(,2600-2400 BP)) found marked humeral asymmetry in Iron Age

males, associated with the use of weapons, but symmetry in Iron Age

females, likely associated with the performance of cereal-processing

PLOS ONE | www.plosone.org 1 November 2014 | Volume 9 | Issue 11 | e112116

http://creativecommons.org/licenses/by/4.0/

http://www.cambridgetrust.org/

http://www.sshrc-crsh.gc.ca/

http://erc.europa.eu/

http://crossmark.crossref.org/dialog/?doi=10.1371/journal.pone.0112116&domain=pdf

activities [21]. In the Americas, pronounced sexual dimorphism in

upper limb diaphyseal morphology has been noted during

agricultural intensification, with male and female behaviors follow-

ing different trends due to the sexual division of labor and/or social

stratification [24–25].

The study of bone adaptation in modern human athletes of

known loading regime has greatly facilitated the interpretation of

complex behavior patterns in the past from skeletal remains. Many

studies of athletes in racquet and throwing sports that produce

bilaterally asymmetrical loading patterns have found greater bone

mineral content, cortical area, total subperiosteal area, and

bending and torsional rigidity in the dominant (loaded) limb

relative to the non-dominant limb [1–13]. In contrast, bilateral

upper limb loading in swimmers has been shown to increase

diaphyseal cross-sectional robusticity relative to controls in both

limbs and is associated with more equal bilateral humeral

robusticity [12]. Bone length has a more limited responsiveness

to loading than do diaphyseal cross-sectional dimensions [26–31],

as it is more genetically canalized and has a limited period during

which adaptation is possible (prior to growth plate closure) [30,32–

33]. Thus, evidence of adaptation in length asymmetry in response

to upper limb loading is not as strong as that for diaphyseal

adaptation. Krahl and colleagues [2] found significant lateraliza-

tion in forearm length and bone diameters in professional tennis

players that was not present in controls, but Haapasalo and

colleagues [5] found no significant difference in length asymmetry

between young tennis players and controls, so loading differences

between young players and controls did not appear to be

impacting bone length.

Expressing an individual’s left and right bone biomechanical

properties as percent asymmetries allows asymmetry to be more

confidently attributed to the local influences of mechanical loading

[34] and removes individual differences in systemic genetic and

hormonal factors that may also affect bone morphology. This is

particularly important when comparing the sexes, as pubertal

testosterone and estrogen drive sex-specific change in the relative

rates of periosteal and endosteal bone deposition and resorption

[35–40], in muscle size/strength [10,29,41–42], and in the timing

of growth plate closure [43–46], all factors which can affect bone

length and/or cross-sectional dimensions.

There have been very few studies of asymmetry in humeral

biomechanical properties or lengths following the introduction of

farming, though see [47]. In Central Europe, variation in the

complexity of grave assemblages and the degree to which

cemeteries have been extensively studied and published means

that more can be gleaned about possible behaviors during life in

some of the region’s cemeteries than in others. However, the

existing Central European archaeological and osteological evi-

dence suggests that changing technologies and divisions of labor

had the potential to impact upper limb loading and asymmetry

through time, particularly between the sexes.

Central Europe from ,5500 BC to ,100ADIn Central Europe, the earliest farmers belonged to the Early

Neolithic Linear Pottery cultures. In much of the region, this was

the Linearbandkeramik (LBK) culture (,5500-4900 BC), charac-

terized by its distinctive pottery style, adze-axe stone tools, and

timber longhouses [48]. LBK farmers practiced mixed farming,

raising domesticated livestock and cultivating and harvesting

cereals prior to metallurgy and mechanization, instead relying on

manual tools like digging sticks and flint sickles [48]. In the Great

Hungarian Plain, east of the Danube in Hungary, the earliest

farmers belonged to the Alfold Linear Pottery (ALP) culture, or

alfoldi vonaldiszes keramia, who shared many cultural features

with the LBK [49].

Sex differences are evident in the dentition of LBK groups,

indicative of dietary differences [49] and at least some division of

tasks by sex [50]. For instance, older LBK females from the well-

studied settlement and cemetery at Vedrovice (Moravia, Czech

Republic) [51–66] as well as Nitra Horne Krskany (western

Slovakia) [63,66] show dental evidence of having used their teeth

as tools, possibly for the working of plant fibers and the production

of cord/rope [50,67]. Pottery is also more often found with female

remains in the Central European Neolithic [68]. In contrast, LBK

males at Schwetzingen (Baden-Wurttemberg, Germany) [69] were

more likely than females to be buried with flint arrowheads [70].

Stone adzes and axes, likely primarily used for woodworking, are

found almost exclusively in male graves in Central Europe,

including at Vedrovice, Schwetzingen, and Nitra Horne Krskany

[63,68]. Not only is the production of adzes/axes labor-intensive

[63], their unilateral use produces similar upper limb movements

and levels of strain as overhead throwing [71]. These sex

differences in grave goods suggest that manipulative activities

may have been quite different between Neolithic men and women

in ways that may be reflected in upper limb asymmetry.

The many innovations in technology and metallurgy of the

Middle/Late Neolithic likely also impacted upper limb loading.

Simple ards were used for cutting shallow furrows in the soil, but

bilateral manual labor with hoes and other implements would still

have been required to first clear the land of brush or cut deeper

furrows if required. Plows that actually turned the soil both

allowed for more difficult soils to be worked and more land to be

exploited [68], likely altering the manipulative behaviors associ-

ated with farming. Ard marks (long thin scratches) dating to the

Middle Neolithic have been found in Central Europe [68,72],

while plow marks become prevalent by the end of the Middle

Neolithic, ,3500 BC [68,73–74]. Early copper mining and

metallurgy likely also had profound impacts on upper limb loading

patterns among males and females. There was already evidence of

copper metallurgy in Middle Neolithic Vinca settlement and burial

contexts (,5000-4460 cal BC) [75], and some Central European

sites show evidence of the mining and smelting of copper ore [68],

including Rudna Glava in Serbia [76]. These activities involved

many unilaterally and bilaterally strenuous tasks with the upper

limbs, such as the hammering and chiseling of ores out of the

surrounding rock and their pounding and grinding prior to

smelting [77].

Throughout the Bronze Age in Central Europe, in addition to

the physical requirements of mining and the production of metal

objects, the increased use of weaponry and the great variety of

tasks in which individuals would have specialized all had the

potential to produce differences in upper limb loading relative to

the preceding Neolithic. By the Early Bronze Age (EBA; ,2300-

1500 cal BC) in Central Europe, metallurgy had intensified

substantially and continued to do so through the Late Bronze Age

(LBA: ,1300-750 cal BC), with significant technological and

socioeconomic consequences [78–79]. At the Early Bronze Age

site of Brno-Turany (Moravia, Czech Republic), several individ-

uals buried in reserve or storage pits on the settlement outskirts,

rather than the more typical location in graves or settlement

features, showed signs of impaired health or trauma, suggesting an

influence of social stratification on burial practices [80]; however,

subsequent analyses did not find any direct relationship between

burial treatment and health status at the site [81].

Throughout the Bronze Age, copper metallurgy continued, with

the novel addition of tin or arsenic to produce bronze, and the

manual activities involved in copper and bronze production would

Manipulative Behavior in Central European Farmers


have been similar. Agriculture also remained of primary impor-

tance in the Bronze Age, though upper limb loading patterns in

the portion of the population involved in farming may have been

altered by the use of ards and plows, querns for grinding grain,

pounders, sickles, and various other implements at this time [82].

Additionally, the rise in prominence of warfare in the Bronze Age

may have been associated with temporal and sex differences in

upper limb loading. A wide range of weapons are found in the

archaeological record at this time, including bows, arrowheads,

daggers, halberds, swords, and spears, accompanied by the

development of defensive armor and the presence of defended

settlements [83]. Weapons are much more common in male

graves than female graves in the Bronze Age, for example [84], so

their production and/or use were probably more often male rather

than female activities. The Bronze Age also brought more

pronounced social stratification and complexity [73,83,85–86],

social changes that are reflected in both the number and prestige

of grave goods in some Central European cemeteries, for example

[84,87]. Bronze Age craft specialization was significant, involving

not just the production of metal objects but of pottery, glass, and

salt, as well as carpentry, the working of leather, bone, and antler,

and the manufacture of textiles from wool and flax [79,83,88].

However, the manipulative activities involved in many of these

crafts would have been similar, as would those involved in the

quarrying and preparation of ores, stone, and flint [88].

The shifting role of metals in society documents a gradual

transition between bronze and iron production. In the Early Iron

Age (,800-450 BC) [89], bronze was still used for weapons and

tools, but as the use of iron in tool manufacture increased, bronze

remained important for personal ornamentation and various

utilitarian items. Though the types of items made from bronze

shifted in the Iron Age, the manipulative activities involved in its

mining, smelting, and smithing would have remained similar [89].

The mining of iron would not have required much change in

method or upper limb loading; however, once iron tools could be

used, overall efficiency likely increased significantly [77]. Iron was

stronger and more widely available than bronze, so could be used

to produce an exceptional variety of tools. Its use in agricultural

implements such as plows, scythes, shovels, and hoes also greatly

increased the efficiency of food production and harvesting [89]. In

addition, the ability to work iron freed communities from a

dependence on more distant and less readily available sources of

other metals typical of the Bronze Age, as iron ore deposits were

ubiquitous and sizeable [77]. Large fortified settlement centers of

significant political and commercial importance formed in the Iron

Age [77], and craft specialization and socioeconomic stratification

were high [90]. Crafts were diverse, including the working of a

variety of metals and the production of pottery [89], and their

assignment would likely have been sex-specific. Warfare was an

important part of Iron Age society in Central Europe, particularly

for men, with a variety of weapons being produced and found in

large numbers in burial, ritual, and settlement contexts [89]. High

social stratification may be interpreted from differential funerary

treatment, access to dietary resources, and stature among Iron Age

Celtic and Scythian males [91–92] and health differences among

Scythian men and women (northeast Hungary) [93]. However, in

terms of upper limb loading, the wide variety of tasks in which

Iron Age individuals were involved, combined with high social

complexity, likely means that variation in the degree to which any

one pattern of strenuous upper limb bone loading predominated

may be reduced relative to earlier groups.

Central European humeral biomechanicsGiven the evidence for considerable social and technological

change following the introduction of agriculture in Central

Europe, it is likely that the type or distribution of habitual

manipulative behaviors among members of the population would

have been affected. Behavioral change may have altered upper

limb loading, and thus may be reflected in humeral morphology.

The mechanical performance of limb bones can be quantified by

the calculation of cross-sectional geometric (CSG) properties,

including estimates of compressive strength (total subperiosteal

area; TA) and bending and torsional rigidity (polar second

moment of area; J) [34,94]. To date there has been only one

published study of temporal change in humeral biomechanics

through this time in past Central European populations. Sladek

and colleagues [47] compared humeral length, cross-sectional

strength, and shape in Late Eneolithic (copper metallurgy) and

EBA groups in Lower Austria, Moravia, and Bohemia. The

authors found that the manipulative behaviors associated with

both copper and bronze metallurgy in this region were similar,

with no significant change in humeral robusticity or its patterns of

asymmetry in either sex. In both time periods, humeral cross-

sectional morphology indicated asymmetrical right-biased loading

in males but little asymmetry in maximum length, while the

situation was reversed in females, with very symmetrical loading

between left and right humeri but right-biased length lateraliza-

tion. This reversed lateralization in length and diaphyseal CSG

properties between the sexes in Central Europe is consistent with

Auerbach and Ruff’s [30] findings in a larger sample of Holocene

adults, which included 151 Neolithic, Bronze Age, Iron Age, and

Early Medieval Europeans.

The current study attempts to elucidate the long-term effects of

agricultural intensification, the introduction and expansion of

metallurgy, and social change on habitual upper limb behaviors

during the first ,5400 years of agriculture in Central Europe. To

do so, asymmetry and variability in humeral maximum lengths

and CSG properties are compared temporally and between the

sexes. Asymmetry and variability are expected to be higher in

CSG properties than in maximum lengths in all time periods. It is

expected that significant differences in upper limb asymmetry and

variability will be found between the Early/Middle Neolithic and

Early/Middle Bronze Age groups, associated with greater

agricultural efficiency, the expansion of mining and copper and

bronze metallurgy, the manufacture and production of metal

objects and other crafts, and the increased task specialization that

accompanied these changes. Given the considerable overlap of

bronze and iron production in Central Europe [90,95], reduced

temporal change in humeral asymmetry between the Early/

Middle Bronze Age and Iron Age groups is expected.

Materials and Methods

Skeletal sampleAll skeletal remains utilized for this research are from

archaeological populations with broadly similar subsistence

patterns, with primary reliance on domesticated crops and

livestock [48], representing portions of three archaeological time

periods following the transition to agriculture: the Early/Middle

Neolithic (,5300-4600 cal BC), Early/Middle Bronze Age

(,2300-1450 BC), and Early through Late Iron Age (,850BC-

100 AD). All remains were originally excavated from southwest

Germany, western Slovakia, Hungary, the Czech Republic, and

northern Serbia (Fig. 1) and are housed in museum and university

collections. No permits were required for the described study,

which complied with all relevant regulations. Sample details on all



Central European cemeteries included in analyses are available in

Table 1, and more detailed specimen information and all relevant

data are presented in Tables S1 and S2.

A total of 174 individuals (96 males, 78 females) had sufficient

preservation of at least one humerus to be included in analyses of

variation in length and CSG properties. Of these, 156 (85 males,

71 females) had paired elements from which asymmetry in CSG

properties could be calculated. In 22 individuals, poor preservation

of proximal or distal joint surfaces in one of the paired humeri

required the estimation of maximum length from the well-

preserved side, leaving 134 pairs of humeri (73 males, 61 females)

for inclusion in analyses of humeral length asymmetry.

Age was estimated and sexes determined according to the

methods outlined in Buikstra and Ubelaker [96]. In order to

reduce the effects of age-related differences in cortical thickness

between individuals on mechanical property estimates [28], only

skeletally mature adults were included in analyses, with preference

given to adults within the approximate age range of ,20–40 years.

However, limitations of sample size and preservation status meant

that this was not always possible.

Silicone moulding and quantification of CSG propertiesCSG properties of left and right humeri were generated using a

silicone moulding method [97–98]. Periosteal moulds were taken

at 35% of maximum humeral length using Coltene President

polyvinyl siloxane putty. Estimates of CSG properties from

periosteal methods have shown a strong correspondence with true

CSG properties derived from both the periosteal and endosteal

contour at the 35% location [98]. In addition, this location has

been used to show strong differences in upper limb loading

between human groups [17–18,99], though it should be noted that

the full range of elbow loading in humans might not necessarily be

reflected at this location [20]. Moulds were then scanned in

anatomical orientation using a flatbed document scanner,

orientated with the x-axis running mediolaterally and the y-axis

running anteroposteriorly. Mould images were imported into

Adobe Photoshop and periosteal contours were traced, creating a

solid cross-sectional image of the humeral shaft. CSG properties

were quantified using BoneJ [100], a bone image analysis plug-in

for ImageJ (http://rsbweb.nih.gov/ij/). Periosteal mould images

do not provide visualization of the endosteal contour; however,

Figure 1. Map of Central Europe with geographical location of cemeteries: 1. Vedrovice 2. Nitra Horne Krskany 3. Schwetzingen 4.Stuttgart-Muhlhausen 5. Polgar-Ferenci-hat 6. Hrtkovci-Gomolava 7. Brno-Turany 8. Polgar Kenderfold 9. Ostojicevo 10. Brno-Malomerice 11. Tapioszele.doi:10.1371/journal.pone.0112116.g001



http://rsbweb.nih.gov/ij/

periosteally-derived CSG properties (such as those quantified from

silicone moulding and laser surface scanning) have shown strong

correspondence with true CSG properties [98,101–103].

The CSG properties analyzed in this study are total subperi-

osteal area (TA) and the polar second moment of area (J). TA is

highly correlated with cortical area and provides a measure of

compressive strength (mm2) [34]. J provides an estimate of

torsional and (twice) average bending rigidity in any two

perpendicular planes through the sum of the second moments of

area for those planes, for instance about anteroposterior (Ix) and

mediolateral (Iy) or maximum (Imax) and minimum (Imin) planes

[34]. In this instance, J was quantified as the sum of Imax and Imin.

Size-standardization of CSG properties was performed following

the method of Ruff [34]: TA/estimated body mass and J/

(estimated body mass * maximum bone length2). Maximum

humeral length parallel to the long axis of the diaphysis was

recorded using an osteometric board, and body mass was

estimated using an average of left and right femoral head

diameters (obtained using sliding calipers) following the equations

for European Holocene populations presented by Ruff and

colleagues [104].

Quantification of humeral asymmetry and variabilityHumeral asymmetries in maximum length and CSG properties

were explored through the conversion of lengths and unstandard-

ized TA and J values into percent directional asymmetries (%DA):

((right-left)/(average of left and right))*100 [30,105–106]. Percent

directional asymmetry provides a measure of both the magnitude

of asymmetry and its direction: positive %DA indicates relative

hypertrophy in the right humerus compared to the left, and vice

versa when %DA is negative. Following Stock and colleagues

[107], a 0% cut-off was used to determine right-bias frequencies

for TA and J; Auerbach and Ruff [30] showed that similar results

were found when 0%, 0.5%, or 1% DA was used as a cut-off

distinguishing handedness from fluctuating asymmetry. However,

three individuals with very low asymmetry (one Iron Age Brno-

Malomerice male, and two Bronze Age females from Ostojicevo

and Brno-Turany) were slightly negative in one property but

slightly positive in the other, resulting in different percentages of

right-bias for TA and J. Variability in maximum length, TA, and Jin both left and right humeri by sex was quantified through the

calculation of coefficients of variation (CV), calculated as (standard

deviation/mean) *100, which provide a size-independent method

for the evaluation of relative variation [108].

Table 1. Central European sample details.

Time Period and Culture ApproximateDate (BC)* CemeteryCemeteryLocation Collection Housed At:

Individuals (males/females)

Neolithic 83 (49/34)

Early

LBK 5300–5100* Vedrovice Czech Republic Moravian Museum (Brno) 18 (6/12)

LBK 5370–4980* Nitra Horne Krskany Slovakia Moravian Museum (Brno) 12 (7/5)

LBK 5260–5010* Schwetzingen Germany Stuttgart Regional Council,State Conservation Office-Osteology (Konstanz)

13 (8/5)

LBK 5200–4960* Stuttgart-Muhlhausen Germany University of Tubingen 22 (13/9)

ALP 5300–5070* Polgar-Ferenci-hat Hungary Hungarian Natural HistoryMuseum (Budapest)

8 (6/2)

Middle

Vinca ,4950–4600* Hrtkovci-Gomolava Serbia Museum of Vojvodina(Novi Sad)

10 (9/1)

Bronze Age 62 (34/28)

Early

Unetice 2300–1700 Brno-Turany Czech Republic Masaryk University (Brno) 12 (8/4)

Maros ,1600/1500 Ostojicevo Serbia National Museum of Kikinda 33 (15/18)

Middle

Fuzesabony 1550–1450 Polgar Kenderfold Hungary Hungarian Natural HistoryMuseum (Budapest)

17 (11/6)

Iron Age 35 (14/21)

Early

Bosut 850–600/500 Hrtkovci-Gomolava Serbia Museum of Vojvodina(Novi Sad)

6 (3/3)

Middle

Celtic 400–200 Brno-Malomerice Czech Republic Moravian Museum (Brno) 14 (4/10)

Late

Scythian 385-100AD* Tapioszele Hungary Hungarian Natural HistoryMuseum (Budapest)

15 (7/8)

* indicates calibrated radiocarbon date; N = number of individuals; LBK = Linearbandkeramik; ALP = Alfold Linear Pottery; dates from: [49, 51 57, 62, 93, 95, 117–118,134, 147], Zdenek Tvrdy, pers. comm.doi:10.1371/journal.pone.0112116.t001



Statistical analysesThe Kruskal-Wallis test was used examine differences in %DA

in maximum length, TA, and J in each sex between time periods

as well as between cemeteries within each time period. Mann-

Whitney tests were also used to test for sex differences in

asymmetry in humeral length, TA, and J within each time period.

A modified Levene’s test for homogeneity of mean-adjusted

absolute deviation scores was used to test for differences in CVs

through time and between the sexes, as these might be indicative

of changing task specialization and the range of activities being

performed among males and females. The total group mean for

each variable was calculated for males and females in each time

period. Each individual’s value for each variable, for example TA,

was then adjusted by his or her group mean using the following

equation, where ABS refers to absolute deviation: ((ABS(TA - total

group mean for TA))/total group mean for TA). The result of this

equation was an absolute deviation value for each individual,

indicating how far each individual’s value was from the group

mean for a given variable (in this example, TA). One-way analysis

of variance (ANOVA) was used to test for temporal change in

these absolute deviation scores adjusted for the mean, in each sex

as well as between the sexes. If the ANOVA indicated a significant

difference between the absolute deviation scores of two groups,

variation between the groups was considered to be significantly

different.

To determine whether or not the percentage of right-biased

individuals for TA and J in each time period was significantly

different from what would be expected by chance, chi-squared

tests were used. Due to the need for both humeral elements to be

well preserved, sample sizes were reduced for the examination of

asymmetry. For this reason, no further statistical analyses were run

on percent right-bias data. All statistical analyses were conducted

in SPSS v20.

Results

Lateralization in humeral length, TA, and JSummary statistics for mean %DAs in humeral length, TA, and

J by time period and sex are presented in Table 2, and by

cemetery and sex in Table 3. Among females, %DA for both TAand J increased significantly from the Bronze Age to the Iron Age

(TA: p,0.034, J: p,0.038; Fig. 2a,b). Low levels of asymmetry

among Bronze Age females are in marked opposition to high

lateralization among Bronze Age males, driving pronounced

sexual dimorphism in %DA in the Bronze Age group overall, in

both TA and J (p,0.001 for both). Among Bronze Age cemeteries,

it was the EBA cemetery of Brno-Turany that particularly drove

high lateralization in J among males: at this cemetery, males had

significantly higher %DA in J (%DA = 19.16%) than males at

either Polgar Kenderfold (%DA = 8.78%; p,0.038) or Ostojicevo

(%DA = 8.79%; p,0.024) (Fig. 3). Percent DA in maximum

length also increased significantly in the Iron Age, in males relative

to both Neolithic (p,0.006) and Bronze Age (p,0.004) males

(Fig. 2c). This length asymmetry among Iron Age males led to a

reduction in the high levels of sexual dimorphism in asymmetry

noted among earlier groups: Neolithic and Bronze Age females

had significantly higher %DA in maximum length than males (p,

0.011 and p,0.001, respectively).

Table 2. Summary statistics for mean percent directional

asymmetries (%DA) by time period and sex.

Table 3. Summary statistics for percent directional asymme-

tries (%DAs) by cemetery and sex.

Due to very low overall percent asymmetries in maximum

length, only percent right bias in TA and J were calculated and

Ta

ble

2.

Sum

mar

yst

atis

tics

for

me

anp

erc

en

td

ire

ctio

nal

asym

me

trie

s(%

DA

)b

yti

me

pe

rio

dan

dse

x.

Tim

eP

eri

od

Se

xT

AJ

Ma

xL

en

gth

NM

ea

nS

DM

ea

nS

DN

Me

an

SD

Ne

oli

thic

Mal

es

50

5.2

45

.09

10

.21

9.9

84

10

.78

0.9

8

Fem

ale

s2

93

.65

4.3

27

.29

8.5

02

81

.51

1.4

4

Bro

nz

eM

ale

s2

56

.20

4.6

81

2.3

79

.28

26

0.7

40

.70

Fem

ale

s2

62

.04

4.0

14

.25

8.0

42

12

.09

1.4

2

Iro

nA

ge

Mal

es

10

5.4

94

.78

10

.86

9.5

46

2.2

96

c1

.09

8

Fem

ale

s1

64

.61

a4

.22

9.0

7b

8.3

81

21

.85

51

.42

3

Max

Len

gth

=m

axim

um

bo

ne

len

gth

incm

s;u

nd

erl

ine

dsu

pe

rscr

ipts

aan

db

ind

icat

esi

gn

ific

antl

yh

igh

er

%D

Ain

Iro

nA

ge

fem

ale

sre

lati

veto

the

Bro

nze

Ag

e(a

:p

,0

.03

4;

b:

p,

0.0

38

);u

nd

erl

ine

dsu

pe

rscr

ipt

cin

dic

ate

ssi

gn

ific

antl

yh

igh

er

%D

Ain

Iro

nA

ge

mal

es

rela

tive

toN

eo

lith

ic(p

,0

.00

6)

and

Bro

nze

Ag

e(p

,0

.00

4)

mal

es;

bo

ldin

dic

ate

ssi

gn

ific

ant

sexu

ald

imo

rph

ism

(TA

and

J:p

,0

.00

1fo

rb

oth

;max

len

gth

:Ne

olit

hic

p,

0.0

11

;Bro

nze

Ag

ep

,

0.0

01

).d

oi:1

0.1

37

1/j

ou

rnal

.po

ne

.01

12

11

6.t

00

2



Ta

ble

3.

Sum

mar

yst

atis

tics

for

me

anp

erc

en

td

ire

ctio

nal

asym

me

trie

s(%

DA

)b

yti

me

pe

rio

dan

dse

x.

Tim

eP

eri

od

Sit

eS

ex

Pe

rce

nt

dir

ect

ion

al

asy

mm

etr

y(%

DA

)

TA

JM

ax

Le

ng

th

NM

ea

nS

DM

ea

nS

DN

Me

an

SD

NEO

LIT

HIC

Ve

dro

vice

M5

6.7

83

.92

14

.06

8.2

43

1.0

80

.27

F1

13

.86

5.5

57

.83

11

.07

1.2

31

.74

Nit

raH

orn

eK

rska

ny

M8

6.4

06

.91

12

.37

13

.40

60

.74

1.2

7

F4

1.3

32

.56

1.4

63

.26

41

.26

0.7

3

Sch

we

tzin

ge

nM

73

.84

1.9

47

.07

3.4

03

20

.38

0.6

7

F3

5.9

41

.66

11

.87

3.4

34

1.1

51

.58

Stu

ttg

art-

Mu

hlh

ause

nM

12

3.9

83

.52

7.5

56

.80

12

0.9

30

.90

F7

5.1

31

.33

10

.50

2.7

71

01

.73

1.2

1

Po

lgar

-Fe

ren

ci-h

atM

63

.77

7.9

67

.58

15

.49

60

.36

0.8

2

F2

2.0

45

.53

4.1

78

.78

22

.08

3.4

4

Hrt

kovc

i-G

om

ola

vaM

10

7.4

13

.95

14

.38

7.9

91

11

.10

1.0

1

F1

5.9

4-

12

.23

-1

2.4

9-

BR

ON

ZE

AG

EB

rno

-Tu

ran

yM

79

.61

4.4

11

9.1

68

.54

51

.09

0.7

0

F5

0.9

94

.31

2.1

48

.32

31

.90

1.6

1

Po

lgar

Ke

nd

erf

old

M4

4.4

92

.47

8.7

84

.88

10

0.6

50

.86

F4

20

.56

2.1

92

0.8

44

.34

42

.68

1.0

4

Ost

ojic

evo

M1

34

.36

4.1

48

.79

8.3

61

10

.65

0.5

3

F1

62

.41

3.4

94

.85

6.8

31

41

.97

1.5

2

IRO

NA

GE

Hrt

kovc

i-G

om

ola

vaM

35

.58

4.6

21

0.8

89

.41

32

.76

0.7

3

F9

3.8

34

.10

7.6

18

.39

71

.72

1.2

9

Brn

o-M

alo

me

rice

M3

5.9

66

.50

12

.40

12

.51

13

.29

-

F3

8.3

35

.99

16

.63

10

.90

--

Tap

iosz

ele

M4

5.0

85

.07

9.7

01

0.2

62

1.1

00

.68

F4

3.5

61

.80

6.6

93

.71

52

.04

1.7

3

M=

mal

e;F

=fe

mal

e;N

=n

um

be

ro

fp

aire

dh

um

eri

;Max

Len

gth

=m

axim

um

bo

ne

len

gth

incm

s;b

old

ind

icat

es

sig

nif

ican

td

iffe

ren

cein

%D

Ain

Jb

etw

ee

nB

ron

zeA

ge

mal

es:

Brn

o-T

ura

ny

sig

nif

ican

tly

hig

he

rth

anO

sto

jice

vo(p

,

0.0

24

)an

dP

olg

arK

en

de

rfo

ld(p

,0

.03

8).

do

i:10

.13

71

/jo

urn

al.p

on

e.0

11

21

16

.t0

03



together these provided a consistent picture through time of

pervasive right-dominance in humeral strength and rigidity

(Fig. 4a,b). Right and left bias frequencies in humeral TA and Jby time period and sex are presented in Table 4. Right-biased

humeral TA and J were significantly greater than would be

expected by chance in both sexes in the Neolithic and Bronze Age

and in Iron Age females, supporting a behavioral component to

this lateralization.

Variability in humeral length, TA, and JCoefficients of variation (CVs) in left and right humeral CSG

properties and maximum length by time period and sex are

presented in Table 5. No temporal change in the variability in any

property was found in left or right humeri in either sex. However,

compared to Neolithic males, Neolithic females had significantly

more variable TA and J in both left and right humeri (Fig. 5a,b;

TA: left humerus p,0.047, right humerus p,0.015; J: left

humerus p,0.006, right humerus p,0.001). Neolithic females

also had slightly higher CVs for maximum length than males, but

not significantly so (p = 0.748 for left humeri, p = 0.842 for right

humeri; Fig. 5c). Though there was no significant sexual

dimorphism in variability in the Bronze Age, the pattern of

variability between the sexes reversed relative to the Neolithic

(Fig. 5); Bronze Age males became more variable than females in

all properties in both humeri (Fig. 6).

Discussion

Neolithic through Bronze Age transitionThis study explores the impact of agricultural intensification,

metallurgy, and social change on habitual manipulative behaviors

through ,5400 years of farming in Central Europe. Mean

asymmetry in TA or J was not significantly different between the

sexes in the Early/Middle Neolithic. The range of %DAs among

Neolithic males and females exhibited considerable overlap, but

Neolithic females had significantly more variable CSG properties

in both left and right humeri than males. Thus, results suggest that

Neolithic females were loading their upper limbs in a wider variety

of ways than males, likely through a broader range of manual

activities, and that these activities generated similar patterns of

lateralization to males (no significant differences in %DA). Women

at the earliest LBK cemetery in Moravia (Czech Republic),

Vedrovice, displayed a wide range of humeral %DAs, while mean

female %DA values at the two early LBK cemeteries from

southwest Germany, Schwetzingen [69,109–110] and Stuttgart-

Muhlhausen [111], were particularly high, especially relative to

males at these sites (see Fig. 3). Early Neolithic females likely

participated in a range of bilateral and unilateral manipulative

activities, related to crop planting/harvesting and the grinding of

grain, gardening, the tending of livestock, the production of

pottery and personal ornamentation, and the working of plant

fibers for rope/cord (based on manipulative tooth wear) [50–51].

Many Neolithic males and females exhibited left-biased or

symmetrical %DA values (see Fig. 2a,b), which could be related

to the two-handed use of tools for grinding grain and/or digging

implements and hoes that would have loaded both limbs. The use

of bimanual digging tools and hoes may even have required

greater loading of the non-dominant limb, similar to the

Figure 2. Percent directional asymmetry in humeral (A) TA, (B)J, and (C) maximum length by time period and sex. Bracketsindicate significant differences (p,0.05 denoted by *; p,0.001 denotedby **).doi:10.1371/journal.pone.0112116.g002



distribution of upper limb loading in bimanual spear use [112–

113].

A small proportion of Neolithic males in the current study had

very high %DA levels outside the range of Neolithic females

(Fig. 2a,b). Thus, at least some males were performing tasks that

heavily loaded their right humerus relative to their left, to an

extent not seen in females. Given that the stone adze-axe is found

almost exclusively in male graves in the Neolithic of Central

Europe [63,66], construction and woodworking utilizing these

tools were likely unilateral tasks more typically performed by Early

Neolithic males. Particularly high %DAs among Neolithic males

were found in two early LBK settlements, Vedrovice in Moravia

(Czech Republic) and Nitra Horne Krskany in western Slovakia,

and the only Middle Neolithic cemetery included, Gomolava in

Vojvodina (Serbia): right-biased directional asymmetry in TA and

J was particularly high in males from these cemeteries (see Table 3

and Figure 3).

Vedrovice was located at the periphery of the earliest expansion

of farming into Central Europe [114–116], with radiocarbon dates

as early as ,5480 cal BC [117], while the earliest date at Nitra is

,5370 cal BC [118]. At this time in the Central European Early

Neolithic, land was still relatively covered in primary forest or

brush, requiring clearance prior to cultivation [48,119]. This was

likely accomplished through burning of the vegetation, but ground

and polished stone adze-axe tools may also have been used for the

clearance of trees, and hoes and digging sticks for the clearance of

brush and digging of furrows. Axes and adzes would also have

been required to procure and work materials in the construction of

the timber longhouses that are characteristic of the early LBK

cultural assemblage [48,120]. The high mean %DA in humeral

CSG properties among some males at these earliest LBK sites in

Central Europe may be related to particularly strenuous use of

adze-axe tools. The forces on the upper limb generated by their

use are high, similar to those generated in sports requiring

overhead throwing [121], and would certainly produce high

unilateral loading in the dominant upper limb. Interestingly,

though adult males at Stuttgart-Muhlhausen did not exhibit such

pronounced right-lateralization in humeral CSG properties, there

are indications that the LBK population at this site may have

loaded their upper limbs to a greater extent than modern humans.

Adults from Stuttgart-Muhlhausen had higher estimated mean

forearm muscle cross-sectional areas (standardized by radius

length) than a sample of 228 living Germans [122], which the

authors interpreted as indicative of higher mechanical loading and

significantly higher muscular activity of the forearm in these early

LBK adults relative to modern humans.

Male mean %DA values in TA and J were also particularly high

at the Vinca site of Gomolava (Middle Neolithic layers) relative to

the Linear Pottery sites of the Early Neolithic (see Table 3 and

Figure 3). There is evidence of copper metallurgy in the Vinca

layers at Gomolava, one of very few known late Vinca cemeteries

in Central Europe, including copper beads, bracelets, and chisels

[123–125]. Mining and smelting of local copper ores in the

Balkans dates back to the fifth millennium BC [126–127] and

would have involved significant loading of the upper limbs. Ore

had to be hammered out of the rock by hand using stone hammers

and antler picks, then crushed up using smaller hand-held

hammers, pestles, and pebble tools, before being roasted,

Figure 3. Percent directional asymmetry in humeral J by cemetery. Sites = Ved: Vedrovice; Nit: Nitra Horne Krskany; Sch: Schwetzingen; Stu:Stuttgart-Muhlhausen; PFH: Polgar-Ferenci-hat; Gom: Hrtkovci-Gomolava (Vinca); BTur: Brno-Turany; PK: Polgar Kenderfold; Ost: Ostojicevo; Gom:Hrtkovci-Gomolava (Bosut); BMal: Brno-Malomerice; Tap: Tapioszele.doi:10.1371/journal.pone.0112116.g003



hammered, and annealed at very high temperatures in shaft

furnaces [78]. The extent to which Gomolava Vinca males were

participating in copper metallurgy, if at all, is unknown, but the

types of activities that produced high unilateral loading were

present at this time, such as those associated with the mining,

smelting, and production of copper objects, and these tasks were

likely male-dominated.

With the Early Bronze Age, significantly higher %DA in TAand J in males relative to females suggests a clear difference in the

degree of symmetrical versus asymmetrical upper limb loading

between the sexes at this time. This pattern was driven primarily

by a reduction in the proportion of females at the high end of

%DA values relative to the Neolithic (see Fig. 2b); the ways that

women’s behaviors loaded their upper limbs changed in the

Bronze Age to a greater extent than did those of men. The

proportion of Bronze Age females performing highly right-biased

loading declined relative to the Neolithic, indicative of greater task

specialization among females and/or a change in the types of

activities performed. Females from the Middle Bronze Age

Fuzesabony cemetery of Polgar Kenderfold (Hungary) [87]

displayed, on average, almost completely symmetrical humeral

TA and J (see Table 3 and Fig. 3).

Not only was loading symmetrical or even left-biased among

Bronze Age females but right-lateralized among Bronze Age

males, this symmetrical female loading was associated with

substantially less variability in CSG properties, driving a reversal

in the sexual dimorphism of humeral variation relative to the

Neolithic period (Fig. 6). These upper limb patterns suggest that

manual activities became more homogeneous among females in

the Bronze Age relative to the Neolithic, with fewer females

participating in strenuous right-biased unilateral tasks. Instead, the

majority of Bronze Age females appear to have been participating

in bilateral manipulative tasks, perhaps the sorting of crushed ores

prior to smelting [77], agricultural fieldwork, the grinding of grains

or ores, and pottery and textile fabrication, which loaded the

upper limbs in similar and symmetrical or left-biased ways. In

contrast, high %DA among Bronze Age males suggests that they

continued to be regularly performing strenuous activities in which

the right upper limb predominated; these could have included

percussive hammering and pounding during mining, smelting, and

smithing, as well as agricultural production and the use of

unilateral weapons.

The most pronounced sex differences in humeral %DA were

found in the Early Bronze Age Unetice settlement and burial site

of Brno-Turany (Moravia, Czech Republic), where male %DA in

humeral J was significantly higher than the slightly later Bronze

Age sites examined and more than nine times greater than mean

female values from the same site (see Table 3 and Fig. 3).

Archaeological and anthropological details of the site of Brno-

Turany were published in 2008 [80]. The site dates to the

Moravian Early Bronze Age (approximately 2300-1700 BC) [54],

a time of major metallurgical expansion and social change [79].

Archaeological finds from the site include bronze hair ornaments

and pottery fragments typical of the Unetice culture [80]. Unetice

graves across Central Europe often contain flint arrowheads and

many metal weapons, such as daggers, flanged axes, and halberds,

indicative of metalworking and weapons use, likely by males, as

well as evidence of spinning, weaving, and pottery, tasks that are

typically female-dominated [88]. It is likely that some of these

activities were being performed at Brno-Turany. A similar pattern

of %DA by sex (high in males and low in females) was identified by

Sladek and colleagues [47] in an Early Bronze Age sample that

included Unetice skeletal remains from Central Europe: mean

female %DA in humeral J was very low (1.06%; below female

means in the current study) compared to that of males (12.78%;

similar to male means in the current study). The authors attributed

this sex-specific pattern of asymmetry in the Early Bronze Age to

the performance of domestic labor among females and their

decreased participation in intensive agriculture.

Sex differences in percent right bias for humeral CSG properties

were most pronounced in the Bronze Age (Fig. 4a,b), where 96%

of males exhibited right dominance in TA/J, compared to just 65%

and 73% of females in the same properties. Humeral CSG

properties were consistently right biased in both sexes in all

Central European agriculturalists studied, but male values in all

time periods fall at the top of the range of modern human values

(the high end of reported right-biasing in modern human humeri is

,90%+) [13] and females at the bottom (the low end of reported

right-biasing in modern humans is ,75%) [28]. For instance, all

males combined (N = 85) demonstrated an overall right bias of

91.8% in humeral J, while in all females combined (N = 71) the

overall right bias was just 73.2%.

Maximum lengths exhibited much lower variability and

asymmetry than CSG properties, though they were consistently

more right-biased in females across both the Neolithic and the

Bronze Age. This was despite significantly higher %DAs in CSG

properties in Bronze Age males relative to females, so asymmetry

in bone length in the Central European groups studied does not

immediately appear to reflect the influence of manipulative

behavior to any large degree. Similarly, Auerbach and Ruff [30]

found no significant correlation between asymmetries in length

and diaphyseal breadth in a wide variety of Holocene humans.

The current study and those of both Auerbach and Ruff [30]

and Sladek and colleagues [47] all noted a similar reversed pattern

of sexual dimorphism in directional asymmetry between humeral

CSG properties and maximum length: right-biased CSG proper-

ties among males were associated with more symmetrical lengths,

and vice versa among females. Strenuous and repetitive move-

ments of the dominant upper limb practiced by athletes in

overhead throwing/hitting sports, such as volleyball, baseball, and

tennis, have been associated with changes in humeral torsion

[128–132] and/or lateral deviations of the distal humerus (valgus

deformity) [133]. Thus, it is possible that higher %DA in CSG

properties combined with lower %DA in lengths may be reflecting

some influence of mechanical loading on deviation or rotation in

the humeral shaft that would indirectly affect length. Additional

factors such as genetic predisposition, sex differences in growth, or

fluctuating asymmetry could also be influencing bone length

asymmetry in Central European agriculturalists.

Bronze Age to Iron Age transitionThe Neolithic through Bronze Age transition in Central Europe

was characterized by divergence in the lateralization of upper limb

loading, pronounced sexual dimorphism, and change in the range

and type of manual activities performed by males and females. In

contrast, the Bronze Age to Iron Age transition in Central Europe

was typified by consistent and significant reductions in the sexual

dimorphism that was characteristic of the Bronze Age. The

current study suggests that the consistency of humeral loading

from the Late Eneolithic to Early Bronze Age noted by Sladek and

colleagues [47] extended into the Iron Age in this region, but only

among males. Lateralization in male humeral CSG properties was

Figure 4. Percent left and right bias in (A) TA and (B) J by time period and sex.doi:10.1371/journal.pone.0112116.g004



Ta

ble

4.

Rig

ht

and

left

bia

sfr

eq

ue

nci

es

inh

um

era

lTA

and

Jb

yti

me

pe

rio

dan

dse

x.

Tim

eP

eri

od

Ma

les

Fe

ma

les

NR

L%

Rp

NR

L%

Rp

TA

Ne

olit

hic

50

44

68

8.0

0,

0.0

01

29

21

87

2.4

0,

0.0

16

Bro

nze

25

24

19

6.0

0,

0.0

01

26

17

96

5.4

0,

0.0

19

Iro

nA

ge

10

91

90

.00

ns

16

14

28

7.5

0,

0.0

03

J Ne

olit

hic

50

44

68

8.0

0,

0.0

01

29

21

87

2.4

0,

0.0

16

Bro

nze

25

24

19

6.0

0,

0.0

01

26

19

77

3.1

0,

0.0

19

Iro

nA

ge

10

10

01

00

.00

ns

16

14

28

7.5

0,

0.0

03

N=

tota

ln

um

be

ro

fp

aire

dh

um

eri

;R

=n

um

be

ro

fin

div

idu

als

wit

hri

gh

t-d

om

inan

ce(+

%D

A);

L=

nu

mb

er

of

ind

ivid

ual

sw

ith

left

-do

min

ance

(-%

DA

);p

valu

es

refl

ect

X2

test

sfo

rsi

gn

ific

ant;

rig

ht-

bia

sin

gre

lati

veto

wh

atw

ou

ldb

ee

xpe

cte

db

ych

ance

;n

s=

no

tsi

gn

ific

ant

atp

,0

.05

.d

oi:1

0.1

37

1/j

ou

rnal

.po

ne

.01

12

11

6.t

00

4

Ta

ble

5.

Hu

me

ral

coe

ffic

ien

tso

fva

riat

ion

(CV

s)b

yti

me

pe

rio

dan

dse

x.

Tim

eP

eri

od

Co

eff

icie

nt

of

Va

ria

tio

n(%

)

Le

ftH

um

eru

sR

igh

tH

um

eru

s

NT

AJ

NM

LN

TA

JN

ML

Ne

oli

thic

Mal

es

48

9.9

01

6.9

06

34

.60

48

9.4

01

5.7

06

14

.60

Fem

ale

s3

21

3.5

02

6.9

04

05

.30

30

13

.30

25

.20

37

5.0

0

Bro

nz

eA

ge

Mal

es

33

10

.90

21

.00

42

5.8

02

81

1.9

02

0.3

04

25

.80

Fem

ale

s2

79

.40

18

.70

33

5.4

02

89

.50

18

.50

32

4.4

0

Iro

nA

ge

Mal

es

12

13

.70

22

.30

26

5.0

01

11

0.5

01

8.2

02

84

.80

Fem

ale

s2

01

2.2

02

1.8

02

34

.90

16

11

.70

19

.30

20

4.8

0

N=

tota

ln

um

be

ro

fh

um

eri

;M

L=

max

imu

mb

on

ele

ng

thin

cms;

bo

ldin

dic

ate

ssi

gn

ific

ant

sexu

ald

imo

rph

ism

inC

V.

(Ne

olit

hic

TA:

left

hu

me

rus

p,

0.0

47

,ri

gh

th

um

eru

sp

,0

.01

5;

Ne

olit

hic

J:le

fth

um

eru

sp

,0

.00

6,

rig

ht

hu

me

rus

p,

0.0

01

).d

oi:1

0.1

37

1/j

ou

rnal

.po

ne

.01

12

11

6.t

00

5



not significantly affected by the incorporation of iron mining and

smelting, iron tool manufacture and use, or social change. In

contrast, Iron Age females exhibited significant increases in %DA

in TA and J relative to the more symmetrical values in Bronze Age

females (Fig. 2a,b), again suggesting that behavioral change

through time affected the upper limb loading of women more

than that of men.

Though Iron Age sample sizes were small, results by cemetery

documented a consistent trend towards increasing mean %DA in

humeral TA and J among females from the Early Bronze Age

through Middle Iron Age (,2300 BC to 200 AD; see Table 3 and

Fig. 3). Based on a range of grave goods associated with the Iron

Age in Central Europe [89] and published finds from Gomolava

and Tapioszele [134–139], it is probable that Iron Age females

were performing a range of manipulative activities associated with

agricultural activities and livestock tending, the production of food,

dairy products, textiles, clothing, personal ornamentation, and

pottery, and various other domestic activities. Iron Age female

humeral CSG properties were not significantly more variable than

those of Bronze Age females in either humerus (see Table 5),

although sample sizes were small and limit the ability to draw

conclusions from this result. In any case, Iron Age females appear

to have loaded their upper limbs significantly more unilaterally

than Early/Middle Bronze Age females, who appear to have been

primarily loading their upper limbs symmetrically.

Lateralized behaviors were particularly interesting in one small

region of Moravia near Brno, Czech Republic: not only did Early

Bronze Age males at Brno-Turany (Unetice) exhibit the highest

%DA in humeral J of all groups sampled (19.16%), but over the

1300+ years between the use of Brno-Turany and Brno-

Malomerice (Celtic) [140–143], average female %DA in both

TA and J increased by approximately eight-fold (see Fig. 3 for J),

though sample sizes are very small. Decorated bronze artifacts

recovered from Brno-Malomerice have been well-documented

[140,144–145], and the cemetery is the largest Celtic burial

ground in Moravia [146]. A larger sample size is required in order

to determine whether or not this high %DA in the three females

examined from Brno-Malomerice was actually the norm at this

site, but results suggest the possibility of population discontinuity

and/or particularly complex changes in division of labor and

social structure in Moravian metallurgical societies.

Significant Neolithic and Bronze Age sexual dimorphism in

humeral maximum length asymmetry (more right-biased in

females) also declined in the Iron Age, through a significant

increase in male length %DAs relative to both preceding periods.

It is not likely that this change in length asymmetry reflects major

changes in the degree of upper limb loading in Iron Age males

relative to previous males, as change in the lateralization of CSG

properties would also be expected if this were the case. However,

high task specialization among Iron Age males may have reduced

the proportion of the population for whom activities would have

involved the repetitive and strenuous overhead rotational motion

(e.g., carpentry, mining, blacksmithing) that may have been

influencing length asymmetry in earlier males.

Figure 5. Coefficients of variation (%) in left and right humeral(A) TA, (B) J, and (C) maximum length in the Neolithic andBronze Age periods by sex. Brackets indicate significant differences(p,0.05 denoted by *; p,0.001 denoted by **).doi:10.1371/journal.pone.0112116.g005



Conclusion

Comparisons of humeral cross-sectional geometry among 174

adults spanning ,5400 years from the onset of agriculture in

Central Europe found that the long-term social change, increasing

task specialization, and the expansion of copper and bronze

metallurgy were associated with little change in upper limb

asymmetry and variation among males but considerable change

among females. These temporal patterns are suggestive of major

changes in the sexual division of labor and the range of manual

activities performed by women through the first ,5400 years of

farming in Central Europe. A major divergence in the lateraliza-

tion of upper limb loading between the sexes occurred in the Early

Bronze Age: female activities that loaded the upper limbs became

more symmetrical and homogeneous relative to the Neolithic. This

may be related to changing agricultural activities among females

with the introduction of the ard and plow and/or the increased

importance of bilaterally symmetrical tasks such as the grinding of

grain, weaving and textile production, and the preparation of

ground ores for smelting. Female upper limb loading became

significantly more right-biased in the Iron Age, likely associated

with the performance of activities involving significant amounts of

unilateral loading. In contrast, males through the entire Central

European sample exhibited consistent right-biased upper limb

lateralization, indicative of the predominance of unilateral upper

limb loading. In the Neolithic, habitual behaviors producing this

type of loading likely included the use of adzes and axes for

woodworking and land clearance, while in the Bronze and Iron

Ages, additional male-dominated unilateral activities would have

included the mining of metal ores and the smelting and production

of metal objects, as well as the use of weapons. In contrast to

diaphyseal cross-sectional geometry, asymmetry and variability in

bone lengths was minimal and was not clearly associated with

mechanical loading.

Supporting Information

Table S1 Sample details and humeral percent direc-tional asymmetries in TA, J, and maximum length for allindividuals.

(XLSX)

Table S2 Sample details and size-standardized TA, J,and maximum lengths of the left and right humeri for allindividuals.

(XLSX)

Acknowledgments

The authors wish to thank the two reviewers whose insightful comments

greatly improved the manuscript. The authors also wish to thank the

following individuals for their hospitality and for access to the skeletal

collections utilized in this research: Michael Francken at the University of

Tubingen (Tubingen, Germany), Joachim Wahl at the University of

Tubingen (Tubingen, Germany) and the Stuttgart Regional Council State

Conservation Office-Osteology (Konstanz, Germany), Lidija Milasinovic at

the National Museum of Kikinda (Kikinda, Serbia), Marija Jovanovic and

Darko Radmanovic at the Museum of Vojvodina (Novi Sad, Serbia), Eva

Drozdova at Masaryk University (Brno, Czech Republic), Zdenek Tvrdy at

the Moravian Museum (Brno, Czech Republic), and Ildiko Pap at the

Hungarian Natural History Museum (Budapest, Hungary). The authors

are grateful to Dr. Emma Pomeroy for her assistance with production of

the map (Figure 1).

Figure 6. Change in the sexual dimorphism of coefficients of variation (CV) in left and right humeral properties between theNeolithic and Bronze Age periods, calculated as the difference between female and male CVs (female CV - male CV).doi:10.1371/journal.pone.0112116.g006



Author Contributions

Conceived and designed the experiments: AAM RP JTS. Performed the

experiments: AAM. Analyzed the data: AAM. Contributed reagents/

materials/analysis tools: AAM RP. Wrote the paper: AAM RP JTS.

Funded the data collection: RP.

References

1. Jones HH, Priest JD, Hayes WC, Tichenor CC, Nagel DA (1977) Humeral

hypertrophy in response to exercise. J Bone Joint Surg Am 59: 204–208.

2. Krahl H, Michaelis U, Pieper HG, Quack G, Montag M (1994) Stimulation of

bone growth through sports. Am J Sports Med 22: 751–757.

3. Ruff CB, Walker A, Trinkaus E (1994) Postcranial robusticity in Homo. III:

Ontogeny. Am J Phys Anthropol 93: 35–54.

4. Kannus P, Haapasalo H, Sankelo M, Sievanan H, Pasanen M, et al. (1995)

Effect of starting age of physical activity on bone mass in the dominant arm of

tennis and squash players. Ann Intern Med 123: 27–31.

5. Haapasalo H, Sievanen H, Kannus P, Heinonen A, Oja P, et al. (1996)

Dimensions and estimated mechanical characteristics of the humerus after

long-term tennis loading. J Bone Miner Res 11: 864–872.

6. Haapasalo H, Kannus P, Sievanen H, Pasanen M, Uusi-Rasi K, et al. (1998)

Effect of long-term unilateral activity on bone mineral density of female junior

tennis players. J Bone Miner Res 13: 310–319.

7. Haapasalo H, Kontulainen S, Sievanen H, Kannus P, Jarvinen M, et al. (2000)

Exercise-induced bone gain is due to enlargement in bone size without a

change in volumetric bone density: A peripheral quantitative computed

tomography study of the upper arms of male tennis players. Bone 27: 351–357.

8. Bass SL, Saxon L, Daly RM, Turner CH, Robling AG, et al. (2002) The effect

of mechanical loading on the size and shape of bone in pre-, peri-, and

postpubertal girls: A study in tennis players. J Bone Miner Res 17: 2274–2280.

9. Kontulainen S, Sievanen H, Kannus P, Pasanen M, Vuori I (2002) Effect of

long-term impact-loading on mass, size, and estimated strength of humerus and

radius of female racquet-sports players: A peripheral quantitative computed

tomography study between young and old starters and controls. J Bone Miner

Res 17: 2281–2289.

10. Ducher G, Courteix D, Meme S, Magni C, Viala JF, et al. (2005) Bone

geometry in response to long-term tennis playing and its relationship with

muscle volume: A quantitative magnetic resonance imaging study in tennis

players. Bone 37: 457–466.

11. Warden SJ, Bogenschutz ED, Smith HD, Gutierrez AR (2009) Throwing

induces substantial torsional adaptation within the midshaft humerus of male

baseball players. Bone 45: 931–941.

12. Shaw CN, Stock JT (2009) Habitual throwing and swimming correspond with

upper limb diaphyseal strength and shape in modern human athletes.

Am J Phys Anthropol 140: 160–172.

13. Shaw CN (2011) Is ’hand preference’ coded in the hominin skeleton? An in-

vivo study of bilateral morphological variation. J Hum Evol 61: 480–487.

14. Weiss E (2003) Effects of rowing on humeral strength. Am J Phys Anthropol

121: 293–302.

15. Bridges PS (1989) Changes in activities with the shift to agriculture in the

southeastern United States. Curr Anthropol 30: 385–394.

16. Hogue SH, Dongarra V (2002) Biomechanical changes in long bone structure:

A study of preagricultural and agricultural populations in northeastern

Mississippi and northwestern Alabama. Midcont J Archaeol 27: 69–88.

17. Sparacello VS, Marchi D (2008) Mobility and subsistence economy: A

diachronic comparison between two groups settled in the same geographical

area (Liguria, Italy). Am J Phys Anthropol 136: 485–495.

18. Marchi D, Sparacello VS, Holt BM, Formicola V (2006) Biomechanical

approach to the reconstruction of activity patterns in Neolithic Western

Liguria, Italy. Am J Phys Anthropol 131: 447–455.

19. Ogilvie MD, Hilton CE (2011) Cross-sectional geometry in the humeri of

foragers and farmers from the prehispanic American Southwest: Exploring

patterns in the sexual division of labor. Am J Phys Anthropol 144: 11–21.

20. Rhodes JA, Knusel CJ (2005) Activity related skeletal change in medieval

humeri: cross-sectional and architecture alterations. Am J Phys Anthropol 128:

536–546.

21. Sparacello VS, Pearson OM, Coppa A, Marchi D (2011) Changes in skeletal

robusticity in an Iron Age agropastoral group: The Samnites from the Alfedena

necropolis (Abruzzo, Central Italy). Am J Phys Anthropol 144: 119–130.

22. Thomas A (2014) Bioarchaeology of the Middle Neolithic: Evidence for

archery among early European farmers. Am J Phys Anthropol 154: 279–290.

23. Krishan K (2011) Marked limb bilateral asymmetry in an agricultural

endogamous population of North India. Am J Hum Biol 23: 674–685.

24. Bridges PS, Blitz JH, Solano MC (2000) Changes in long bone diaphyseal

strength with horticultural intensification in west-central Illinois. Am J Phys

Anthropol 112: 217–238.

25. Wescott DJ, Cunningham DL (2006) Changes in Arikara humeral and femoral

cross-sectional geometry associated with horticultural intensification. J Arch-

aeol Sci 33: 1022–1036.

26. Biewener AA, Bertram JEA (1993) Mechanical loading and bone growth invivo. In: Hall BK, editor.Bone, vol. 7. Boca Raton: CRC Press. pp 1–36.

27. Biewener AA, Bertram JEA (1994) Structural response of growing bone to

exercise and disuse. J Appl Physiol 76: 946–955.

28. Trinkaus E, Churchill SE, Ruff CB (1994) Postcranial robusticity in Homo. II:

Humeral bilateral asymmetry and bone plasticity. Am J Phys Anthropol 93:

1–34.

29. Ruff CB (2003) Growth in bone strength, body size, and muscle size in a

juvenile longitudinal sample. Bone 33: 317–329.

30. Auerbach BM, Ruff CB (2006) Limb bone bilateral asymmetry: Variability and

commonality among modern humans. J Hum Evol 50: 203–218.

31. Blackburn A (2011) Bilateral asymmetry of the humerus during growth and

development. Am J Phys Anthropol 145: 639–646.

32. Sumner DR, Andriacchi TP (1996) Adaptation to differential loading:

Comparison of growth-related changes in cross-sectional properties of the

human femur and humerus. Bone 19: 121–126.

33. Humphrey LT (1998) Growth patterns in the modern human skeleton.

Am J Phys Anthropol 105: 57–72.

34. Ruff CB (2008) Biomechanical analyses of archaeological human skeletal

samples. In: Katzenberg MA, Saunders SR, editors. Biological anthropology of

the human skeleton 2nd ed. New Jersey: John Wiley & Sons. pp 183–206.

35. Garn SM (1970) The earlier gain and the later loss of cortical bone, in

nutritional perspective. Springfield: Charles C. Thomas. 146 p.

36. Garn SM (1972) The course of bone gain and the phases of bone loss. Orthop

Clin North Am 3: 503–520.

37. Libanati C, Baylink DJ, Lois-Wenzel E, Srinivasan N, Mohan S (1999) Studies

on the potential mediators of skeletal changes occurring during puberty in girls.

J Clin Endocrinol Metab 84: 2807–2814.

38. Schoenau E, Neu CM, Rauch F, Manz F (2001) The development of bone

strength at the proximal radius during childhood and adolescence. J Clin

Endocrinol Metab 86: 613–618.

39. Seeman E (2003) Periosteal bone formation— A neglected determinant of bone

strength. N Engl J Med 349: 320–323.

40. Gosman JH, Stout SD, Larsen CS (2011) Skeletal biology over the life span: A

view from the surfaces. Am J Phys Anthropol 146: 86–98.

41. Heinonen A, McKay HA, Whittall KP, Forster BB, Khan KM (2001) Muscle

cross-sectional area is associated with specific site of bone in prepubertal girls: A

quantitative magnetic resonance imaging study. Bone 29: 388–392.

42. Daly RM, Saxon L, Turner CH, Robling AG, Bass SL (2004) The relationship

between muscle size and bone geometry during growth and in response to

exercise. Bone 34: 281–287.

43. Tupman GS (1962) A study of bone growth in normal children and its

relationship to skeletal maturation. J Bone Joint Surg 44B: 42–67.

44. Jansson JO, Eden S, Isaksson O (1983) Sites of action of testosterone and

estradiol on longitudinal bone growth. Am J Physiol Endocrinol Metab 244:

E135–E140.

45. Mauras N, Rogol AD, Haymond MW, Veldhuis JD (1996) Sex steroids, growth

hormone, insulin-like growth factor-I: Neuroendocrine and metabolic regula-

tion in puberty. Horm Res Paediatr 45: 74–80.

46. Cutler GB (1997) The role of estrogen in bone growth and maturation during

childhood and adolescence. J Steroid Biochem Mol Biol 61: 3–6.

47. Sladek V, Berner M, Sosna D, Sailer R (2007) Human manipulative behavior

in the Central European Late Eneolithic and Early Bronze Age: humeral

bilateral asymmetry. Am J Phys Anthropol 133: 669–681.

48. Milisauskas S (2002) Early Neolithic: The first farmers in Europe, 7000-5500/

5000 BC. In: Milisauskas S, editor. European prehistory: A survey. New York:

Kluwer Academic. pp 143–192.

49. Whittle A, Anders A, Bentley RA, Bickle P, Cramp L, et al. (2013) Hungary.

In: Bickle P, Whittle A, editors. The first farmers of Central Europe: Diversity

in LBK lifeways. Oxford:Oxbow Books. pp 49–100.

50. Frayer DW (2004) The dental remains from Krskany (Slovakia) and Vedrovice

(Czech Republic). Anthropologie 42: 71–103.

51. Podborsky V (1993) Praveke dejiny Moravy. Brno: Muzejnı a Vlastivdna

Spolecnost v Brne. 543 p.

52. Podborsky V (2002) Dve pohrebiste Neolitickeho lidu s linearnı keramikou ve

Vedrovicıch na Morave. Brno: Ustav archeologie a muzeologie filosoficke

fakulty Masarykovy Univerzity. 343 p.

53. Humpolova A, Ondrus V (1999) Vedrovice, okres Znojmo. In: Podborsky V,

editor. Praveka sociokulturnı architektura na Morave. Brno: Ustav archeologie

a muzeologie filosoficka fakulta Masarykovy univerzity. pp 167–219.

54. Humpolova A (2001) Rondeloid cıslo III lidu s Moravskou malovanou

keramikou ve Vedrovicıch. In: Podborsky V, editor. 50 let archeologicky ch vy

zkumu Masarykovy univerzity na Znojemsku.Brno:Ustav archeologie a

muzeologie filosoficka fakulta Masarykovy univerzity. pp 157–166.

55. Ondrus V (2002) Dve pohrebiste Lidu s Neolitickou linearnı keramikou ve

Vedrovicıch. In: Podborsky V, editor. Dve pohrebiste Neolitickeho lidu s

linearnı keramikou ve Vedrovicıch na Morave. Brno:Ustav archeologie a

muzeologie filosoficka fakulta Masarykovy univerzity. pp .9–122



56. Smrcka V, Buzek F, Erban V, Berkovec T, Dockalova M, et al. (2005) Carbon,

nitrogen and strontium isotopes in the set of skeletons from the Neolithicsettlement at Vedrovice. Anthropologie 43: 315–323.

57. Smrcka V, Mihaljevic M, Zobcova J, Humpolova A, Berkovec T (2006)

Multielementarnı chemicka analyza z kosternıch pozustatku lidı a zvırat

neolitickeho sıdliste ve Vedrovicıch (Ceska Republika). Ve Sluzbach Arche-

ologie 7: 329–340.

58. Dockalova M (2008) Anthropology of the Neolithic population from Vedrovice

(Czech Republic). Anthropologie 46: 239–315.

59. Lillie M (2008) Vedrovice: Demography and paleopathology in an early

farming population. Anthropologie 46: 135–152.

60. Jarosova I (2008) Dietary inferences using buccal microwear analysis on the

LBK population from Vedrovice, Czech Republic. Anthropologie 46: 175–184.

61. Richards MP, Montgomery J, Nehlich O, Grimes V (2008) Isotopic analysis ofhumans and animals from Vedrovice. Anthropologie 46: 185–194.

62. Zvelebil M, Pettitt P (2008) Human condition, life, and death at an early

Neolithic settlement: Bioarchaeological analyses of the Vedrovice cemetery and

their biosocial implications for the spread of agriculture in Central Europe.

Anthropologie 46: 195–218.

63. Bentley RA, Bickle P, Fibiger L, Nowell GM, Dale CW, et al. (2012)

Community differentiation and kinship among Europe’s first farmers. P Natl

Acad Sci 109: 9326–9330.

64. Zvelebil M, Pettitt P (2013) Biosocial archaeology of the Early Neolithic:Synthetic analyses of a human skeletal population from the LBK cemetery of

Vedrovice, Czech Republic. J Anthropol Archaeol 32: 313–329.

65. Skutil J (1941) Linearkeramische Graber in Mahren. Wiener Prahistorische

Zeitschrift 28: 21–37.

66. Pavuk J (1972) Neolithisches Graberfeld in Nitra. Slovenska Archeologia 20: 5–

105.

67. Jarasova I, Dockalova M (2008) Dental remains from the Neolithic settlements

in Moravia, Czech Republic. Anthropology 46: 77–101.

68. Milisauskas S, Kruk J (2002) Middle Neolithic continuity, diversity,

innovations, and greater complexity, 5500/5000-3500/3000 BC. In: Mili-

sauskas S, editor. European prehistory: A survey.New York: Kluwer Academic.

pp 193–246.

69. Gerling C, Francken M (2007) Das linearbankeramische Graberfeld von

Schwetzingen. Archaologische Informationen 30: 43–50.

70. Bentley RA, Bickle P, Francken M, Gerling C, Hamilton J, et al. (2013) Baden-

Wurttemberg. In: Bickle P and Whittle A, editors. The first farmers of Central

Europe: Diversity in LBK lifeways. pp 251–288.

71. Villotte S, Knusel CJ (2014) "I sing of arms and of a man. ": Medial

epicondylitis and the sexual division of labor in Prehistoric Europe. J Arch Sci

43: 168–174.

72. Pleinerova I (1981) Problem stop orby v casne eneolitickem nalezu z Brezna.Archeologicke rozhledy 23: 133–141.

73. Shennan SJ (1993) Settlement and social change in Central Europe. J World

Prehist 7: 121–161.

74. Sherratt A (1981) Plough and pastoralism: Aspects of the Secondary Products

Revolution. In: Hodder I, Isaac G, Hammond N, editors. Pattern of the

past.Cambridge: Cambridge University Press. pp 261–305.

75. Boric D (2009) Absolute dating of metallurgical innovations in the Vinca

culture of the Balkans. In: Kienlin TL, Roberts BW, editors. Metals andSocieties: Studies in honour of Barbara S.Ottaway.Bonn: Habelt. pp 191–245.

76. Jovanovic B (1982) Rudna Glava. Najstarije rudarstvo bakra na centralnom

Balkanu. Bor/Beograd: Muzej Rudarstva I Metalurgie/Arheoloski Institut, knj

17. 155 p.

77. Craddock PT (1995) Early metal mining and production. Edinburgh:

Edinburgh University Press Ltd. 383 p.

78. Stadler P (1999) Ein Beitrag zur Absolutchronologie des Neolithikums afgrund

der 14C-Daten in Osterreich. In: Lenneis E, Neugebauer-Maresch C, Ruttkay

E, editors. Jungsteinzeit im Osten Osterreichs.Vienna: Verlag Niederosterrei-chisches Pressehaus. pp 210–224.

79. Harding A (2002) The Bronze Age. In: Milisauskas S, editor. European

prehistory: A survey.New York:Kluwer Academic. pp 271–334.

80. Kala J, Konasova K, Smrcka V (2008) Pohrby ze zasobnıch jam na okrajiunetickeho pohrebiste v Brne-Turanech. In: Stuchlık S, Ghosh V, Janak V,

editors. Acta Archaeologica Opaviensia. Opava:Ustav historickych ved FPF

Slezske Univerzity v Opave. pp 61–78.

81. Pankowska A (2009) Comparison of health status in human skeletal remains

disposal in settlements and necropolises in the early Bronze Age (in CentralMoravia, Czech Republic). Anthropologie 46: 215–228.

82. Harding A (1976) Bronze agricultural implements in Bronze Age Europe

Sieveking G de G, Longworth I H, Wilson K E, editors. In:Problems in

economic and social archaeology.London: Duckworth. pp 513–522.

83. Harding A (2000) European societies in the Bronze Age. Cambridge:

Cambridge University Press. 572 p.

84. Milasinovic L (2009) Review on possibility of social structure reconstruction on

the Maros culture finds from the necropolis at Ostojicevo. English summary.Rad Muzeja Voyvodina 51: 65–70.

85. Gilman A (1981) The development of social stratification in Bronze Age

Europe. Curr Anthropol 22: 1–23.

86. Bintliff J (1984) European social evolution, archaeological perspectives.Bradford: University of Bradford. 304 p.

87. Dani J, Mathe M, Szabo G (2001) Ausgrabungen in der bronzezeitlichen Tell-Siedlung und im Graberfeld von Polgar-Kenderfold (Vorbericht uber die

Freilegung des mittelbronzezeitlichen Graberfeldes von Polgar-Kenderfold,

Majoros-Tanya). In: Kacso C, editor. Bronzezeitliche Kulturerscheinungen imKarpatischen Raum. Die Beziehungen zu den benachbarten Gebieten.

Ehrensymphosium fur Alexandru Vulpe zum 70. Geburtstag, Baia MareOktober 10-13, 2001. pp 93–118.

88. Coles JM, Harding AF (1979) The Bronze Age in Europe: An introduction to

the prehistory of Europe c. 2000-700 BC. London: Methuen. 581 p.

89. Wells PS (2002) The Iron Age. In: Milisauskas S, editor. European prehistory:

A survey.New York: Kluwer Academic. pp 335–383.

90. Collis J (1984) The European Iron Age. London: Routledge. 192 p.

91. Rolle R (1989) The world of the Scythians. Berkeley and Los Angeles:University of California Press. 141 p.

92. Le Huray JD, Schutkowski H (2005) Diet and social status during the La Tene

period in Bohemia: carbon and nitrogen stable isotope analysis of bonecollagen from Kutna Hora-Karlov and Radovesice. J Anthropol Archaeol 24:

135–147.

93. Ubelaker DH, Pap I (1998) Skeletal evidence for health and disease in the IronAge of Northeastern Hungary. Int J Osteoarchaeol 8: 231–251.

94. Ruff CB, Hayes WC (1983) Cross-sectional geometry of Pecos Pueblo femoraand tibiae—A biomechanical investigation: I. Method and general patterns of

variation. Am J Phys Anthropol 60: 359–381.

95. Tasic N (2003–2004) Historical picture of development of Bronze Age culturesin Vojvodina. Starinar 53–54: 25–34.

96. Buikstra JE, Ubelaker DH (1994) Standards for data collection from human

skeletal remains. Fayetteville: Arkansas Archeological Survey Research SeriesNo. 44. 272 p.

97. Stock JT (2002) A test of two methods of radiographically deriving long bone

cross-sectional properties compared to direct sectioning of the diaphysis.Int J Osteoarch 12: 335–342.

98. Stock JT, Shaw CN (2007) Which measures of diaphyseal robusticity are

robust? A comparison of external methods of quantifying the strength of longbone diaphyses to cross-sectional geometric properties. Am J Phys Anthropol

134: 412–423.

99. Stock JT, Pfeiffer SK (2004) Long bone robusticity and subsistence behaviouramong Later Stone Age foragers of the forest and fynbos biomes of South

Africa. J Archaeol Sci 31: 999–1013.

100. Doube M, Klosowski MM, Arganda-Carreras I, Cordelieres FP, DoughertyRP, et al. (2010) BoneJ: Free and extensible bone image analysis in ImageJ.

Bone 47: 1076–1079.

101. Sparacello VS, Pearson OM (2010) The importance of accounting for the area

of the medullary cavity in cross-sectional geometry: A test based on the femoral

midshaft. Am J Phys Anthropol 143: 612–624.

102. Davies TG, Shaw CN, Stock JT (2012) A test of a new method and software for

the rapid estimation of cross-sectional geometric properties of long bone

diaphyses from 3D laser surface scans. Archaeol Anthropol Sci 4: 277–290.

103. Macintosh AA, Davies TG, Ryan TM, Shaw CN, Stock JT (2013) Periosteal

versus true cross-sectional geometry: A comparison along humeral, femoral,

and tibial diaphyses. Am J Phys Anthropol 150: 442–452.

104. Ruff CB, Holt BM, Niskanen M, Sladek V, Berner M, et al. (2012) Stature and

body mass estimation from skeletal remains in the European Holocene.Am J Phys Anthropol 148: 601–617.

105. Steele J, Mays S (1995) Handedness and directional asymmetry in the long

bones of the human upper limb. Int J Osteoarch 5: 39–49.

106. Mays S (2002) Asymmetry in metacarpal cortical bone in a collection of Britishpost-mediaeval human skeletons. J Archaeol Sci 29: 435–441.

107. Stock JT, Shirley MK, Sarringhaus LA, Davies TG, Shaw CN (2013) Skeletal

evidence for variable patterns of handedness in chimpanzees, human hunter-gatherers, and recent British populations. Ann NY Acad Sci 1288: 86–99.

108. Buck LT, Stock JT, Foley RA (2010) Levels of intraspecific variation within the

catarrhine skeleton. Int J Primatol 31: 779–795.

109. Gerling C (2009) Schwetzingen, ein ’regulares’ Graberfeld der jungeren

Linearbandkeramik. In: Zeeb-Lanz A, editor. Krisen-Kulturwandel-Kontinui-taten.Zum Ende der Bandkeramik in Mitteleuropa.Beitrage der internationalen

Tagung in Herxheim bei Landau (Pfalz) vom 14-17.06.2007.Rahden: Marie

Leidorf. pp 103–110.

110. Nieszery N (1995) Linearbandkeramische Graberfelder in Bayern. Inter-

nationale Archaologie 16. 404 p.

111. Price TD, Wahl J, Knipper C, Burger-Heinrich E, Kurz G, et al. (2003) Dasbandkeramische Graberfeld von Stuttgart-Muhlhausen: Neue Untersuchung-

sergebnisse zum Migrationsverhalten im fruhen Neolithikum. In: Funda, DT,

editor. Fundberichte aus Baden-Wurttemberg.Stuttgart: KommissionsverlagKonrad Theiss Verlag. pp 23–58.

112. Schmitt D, Churchill SE, Hylander WL (2003) Experimental evidenceconcerning spear use in Neandertals and early modern humans. J Archaeol

Sci 30: 103–114.

113. Shaw CN, Hofmann CL, Petraglia MD, Stock JT, Gottschall JS (2012)Neandertal humeri may reflect adaptation to scraping tasks, but not spear

thrusting. PLOS ONE 7: e40349. doi: 10.1371/journal.pone.0040349

114. Zvelebil M (2000) The social context of the agricultural transition in Europe.In: Renfrew C, Boyle K, editors. Archaeogenetics: DNA and the population

prehistory of Europe. Cambridge: McDonald Institute Monographs. pp 57–

79.



115. Zvelebil M (2004) Conclusion: The many origins of the LBK. In: Lukes A,

Zvelebil M, editors. LBK Dialogues: Studies in the formation of the Linear

Pottery Culture.BAR International Series 1304. Oxford: Archaeopress.

pp 183–205.

116. Lukes A, Zvelebil M, Pettitt P (2008) Biological and cultural identity of the first

farmers: Introduction to the Vedrovice Bioarchaeology Project. Anthropologie

46: 117–124.

117. Pettitt P, Hedges R (2008) The age of the Vedrovice cemetery: The AMS

radiocarbon dating programme. Anthropologie 46: 125–134.

118. Whittle A, Bentley RA, Bickle P, Dockalova M, Fibiger L, et al. (2013) Moravia

and western Slovakia. In: Bickle P, Whittle A, editors. The first farmers of

Central Europe: Diversity in LBK lifeways.Oxford:Oxbow Books. pp 101–158.

119. Whittle A (1996) Europe in the Neolithic: The creation of new worlds.

Cambridge: Cambridge University Press. 460 p.

120. Bentley RA (2012) Mobility and the diversity of early Neolithic lives: Isotopic

evidence from skeletons. J Anthropol Archaeol 32: 303–312.

121. Galloway M, DeMaio M, Mangine R (1992) Rehabilitative techniques in the

treatment of medial and lateral epicondylitis. Orthopedics 15: 1089–1096.

122. Slizewski A, Burger-Heinrich E, Francken M, Wahl J, Harvati K (2014) Pilot

study for the reconstruction of soft tissues: Muscle cross-sectional area of the

forearm estimated from cortical bone for a Neolithic sample. The Anat Rec

297: 1103–1114.

123. Boric D (1996) Social Dimensions of Mortuary Practices in the Neolithic: A

Case Study. Starinar 47: 67–83.

124. Brukner B (1980) Naselje vincanske grupe na Gomolavi (neolitski i

ranoeneolitski sloj). Izvestaj sa iskopavanja 1967–1976. Rad Vojvodjanskih

Muzeja 26: 5–55.

125. Ottaway BS (1979) Analysis of earliest metal finds from Gomolava. Rad

Vojvodanskih Muzeja 25: 53–59.

126. Boric D (2009) Absolute dating of metallurgical innovations in the Vinca

culture of the Balkans. In: Kienlin TL, Roberts BW, Metals and societies:

Studies in honour of Barbara S.editors. Ottaway.Universitatsforschungen zur

prahistorischen Archaologie.Bonn: Habelt. pp 191–245.

127. Gale NH, Stos-Gale Z, Raduncheva A, Panayotov I, Ivanov I, et al. (2003)

Early metallurgy in Bulgaria. In: Craddock P, Lang J, editors. Mining and

metal production through the ages. London:The British Museum Press.

pp 122–173.

128. Pieper HG (1998) Humeral torsion in the throwing arm of handball players.

Am J Sport Med 26: 247–253.

129. Osbahr DC, Cannon DL, Speer KP (2002) Retroversion of the humerus in the

throwing shoulder of college baseball pitchers. Am J Sports Med 30: 347–353.

130. Whiteley R, Ginn K, Nicholson L, Adams R (2006) Indirect ultrasound

measurement of humeral torsion in adolescent baseball players and nonathleticadults: reliability and significance. J Sci Med Sport 9: 310–318.

131. Tayler RE, Zheng C, Jackson RP, Doll JC, Chen JC, et al. (2007) The

phenomenon of twisted growth: Humeral torsion in dominant arms of highperformance tennis players. Comput Method Biomec 12: 83–93.

132. Schwab LM, Blanch P (2009) Humeral torsion and passive shoulder range inelite volleyball players. Phys Ther Sport 10: 51–56.

133. Caine EL, Dugas JR, Wolf RS, Andrews JR (2003) Elbow injuries in throwing

athletes: a current concepts review. Am J Sports Med 31: 621–635.134. Tasic N (1972) An Early Iron Age collective tomb at Gomolava. Archaologia

Iugoslavica 13: 27–37.135. Jacobi G (1974) Werkzeug und Gerat aus dem Oppidum von Manching.

Wiesbaden: Franz Steiner. 368 p.136. Fothi E, Zsolt B, Sandor E (2006) A Tapioszelei szkıta kori temeto embertani

vizsgalata. In: Moro G, editor. Az aranyszarvas nyomaban: A Blaskovich

fiverek es a magyar regeszet kapcsolata. Tapioszele: Blaskovich Muzeum BaratiKore. pp 65–93.

137. Parducz M (1966) The Scythian Age Cemetery at Tapioszele. ActaArchaeologica 18: 39–82.

138. Bottyan A (1955) Szkıtak a magyar Alfoldon. Regeszeti Fuzetek 1. Budapest:

Magyar Nemzeti Muzeum.80 pp139. Blaskovich J, Blaskovich G (1958) Tapioszele. Archaeologiai Ertesıto 85: 202.

140. Cizmarova J (2005) Keltske pohrebiste v Brne-Malomericıch/Das keltischeGraberfeld in Brno-Malomerice. Brno:Pravek supplementum14 . 226 p.

141. Poulık J (1942) Das keltische Graberfeld von Brunn-Malmeritz. Zeitschrift desMahrischen Landesmuseums 2: 49–86.

142. Dacık T (1983) Prıspevek k antropologii Keltu na Morave. Archeologicke

rozhledy 35: 496–509.143. Trubacova T (2005) Rozbor antropologickeho materialu. In: Cizmarova J,

editor. Keltske pohrebiste v Brne-Malomericıch/Das keltische Graberfeld inBrno-Malomerice. Brno: Pravek supplementum 14. pp 27–40.

144. Megaw JVS (1970) Art of the European Iron Age. Bath: Adams and Dart. 195 p.

145. Kruta V (2007) La cruche celte de Brno. Chef-d’oeuvre de l’art. Dijon: Miroirde l’Univers. 137 p.

146. Dreslerova G (2005) Vyhodnocenı zvırecıch kostı. Brno:Ustav archeologickepamatkove pece Brno. Pravek Supplementum 142p.

147. Fischl KP, Kiss V, Kulcsar G, Szeverenyi V (2013) Transformations in theCarpathian Basin around 1600 B. C. In:Meller H, editor. 1600 BC – Cultural

change in the shadow of the Thera-Eruption? Halle: Landesamt fu&ur

Denkmalpflege und Archaologie Sachsen-Anhalt - Landesmuseum fu&urVorgeschichte. pp 355–372.



Divergence in Male and Female Manipulative Behaviors with the Intensification of Metallurgy in...

Documents

Transcript of Divergence in Male and Female Manipulative Behaviors with the Intensification of Metallurgy in...